Abstract
Key message
The physiological responses of nine commonly planted North-American hybrid poplars to drought was evaluated, resulting in a ranking of drought resistance. Indicator genes for drought response processes were scored for differences in expression levels in the most sensitive and resistant clones, confirming levels of drought stress and differences consistent with roles in drought resistance.
Abstract
Poplar hybrids are cultivated in North America for environmental applications, agroforestry, and the pulp and paper industry primarily because of their fast growth and limited nutrient requirement. For the same reasons, they have been identified as suitable species for carbon sequestration and as a potential feedstock for carbon–neutral production of energy. The clones deployed on the Canadian prairies are generally regarded as drought sensitive, which poses a problem as water availability has steadily decreased in this region over the past century and a severe water crisis has been predicted. To approach this problem, we tested nine commonly deployed North-American hybrid poplars, developed for large-scale cultivation in the Canadian prairies, for their physiological responses to drought, resulting in a ranking of drought resistance. The difference between the clones showing the most and the least response of drought stress was large, and we used these clones to further examine the differences in the expression of genes known to be up-regulated in response to drought stress. This interrogation showed significant differences in transcript abundance that largely reflected the physiological status of the tested clones, but also many genes being down rather than up-regulated in response to drought stress in the drought-tolerant clone. In particular, putative positive and negative regulators of abscisic acid signaling were expressed at levels consistent with a potential role in observed differences in drought resistance.
Similar content being viewed by others
References
Anderson JE, McNaughton SJ (1973) Effects of low soil temperature on transpiration, photosynthesis, leaf relative water content, and growth among elevationally diverse plant populations. Ecology 54:1220–1233. https://doi.org/10.2307/1934185
Arango-Velez A, Zwiazek JJ, Thomas BR, Tyree MT (2011) Stomatal factors and vulnerability of stem xylem to cavitation in poplars. Physiol Plant 143:154–165. https://doi.org/10.1111/j.1399-3054.2011.01489.x
Arshad M, Mattsson J (2014) A putative poplar PP2C-encoding gene negatively regulates drought and abscisic acid responses in transgenic Arabidopsis thaliana. Trees 28:531–543. https://doi.org/10.1007/s00468-013-0969-7
Balatinecz JJ, Kretschmann DE, Leclercq A (2001) Achievements in the utilization of poplar wood - Guideposts for the future. For Chron 77:265–269. https://doi.org/10.5558/tfc77265-2
Balcke GU, Handrick V, Bergau N et al (2012) An UPLC-MS/MS method for highly sensitive high-throughput analysis of phytohormones in plant tissues. Plant Methods 8:47. https://doi.org/10.1186/1746-4811-8-47
Bartels D, Sunkar R (2005) Drought and salt tolerance in plants. CRC Crit Rev Plant Sci 24:23–58. https://doi.org/10.1080/07352680590910410
Blake TJ, Tschaplinski TJ, Eastham A (1984) Stomatal control of water use efficiency in poplar clones and hybrids. Can J Bot 62:1344–1351. https://doi.org/10.1139/b84-182
Butnar I, Rodrigo J, Gasol CM, Castells F (2010) Life-cycle assessment of electricity from biomass: case studies of two biocrops in Spain. Biomass Bioenerg 34:1780–1788. https://doi.org/10.1016/j.biombioe.2010.07.013
Carsjens C, Ngoc QN, Guzy J et al (2014) Intra-specific variations in expression of stress-related genes in beech progenies are stronger than drought-induced responses. Tree Physiol 34:1348–1361. https://doi.org/10.1093/treephys/tpu093
Chen J, Song Y, Zhang H, Zhang D (2013) Genome-wide analysis of gene expression in response to drought stress in Populus simonii. Plant Mol Biol Report 31:946–962. https://doi.org/10.1007/s11105-013-0563-6
Cohen D, Bogeat-Triboulot M-B, Tisserant E et al (2010) Comparative transcriptomics of drought responses in Populus: a meta-analysis of genome-wide expression profiling in mature leaves and root apices across two genotypes. BMC Genom 11:630. https://doi.org/10.1186/1471-2164-11-630
DesRochers A, van den Driessche R, Thomas BR (2007) The interaction between nitrogen source, soil pH, and drought in the growth and physiology of three poplar clones. Can J Bot 85:1046–1057. https://doi.org/10.1139/B07-062
Dickmann DI, Isebrands JG, Eckenwalder JE, Richardson J (eds) (2002) Poplar culture in North America. NRC Research, Ottawa
Gebre GM, Kuhns MR, Brandle JR (1994) Organic solute accumulation and dehydration tolerance in three water-stressed Populus deltoides clones. Tree Physiol 14:575–587. https://doi.org/10.1093/treephys/14.6.575
González-García S, Gasol CM, Gabarrell X et al (2010) Environmental profile of ethanol from poplar biomass as transport fuel in Southern Europe. Renew Energy 35:1014–1023. https://doi.org/10.1016/j.renene.2009.10.029
Guidolotti G, Calfapietra C, Loreto F (2011) The relationship between isoprene emission, CO2 assimilation and water use efficiency across a range of poplar genotypes. Physiol Plant 142:297–304. https://doi.org/10.1111/j.1399-3054.2011.01463.x
Hacke UG, Plavcová L, Almeida-Rodriguez A et al (2010) Influence of nitrogen fertilization on xylem traits and aquaporin expression in stems of hybrid poplar. Tree Physiol 30:1016–1025. https://doi.org/10.1093/treephys/tpq058
Hamanishi ET, Raj SH, Wilkins O et al (2010) Intraspecific variation in the Populus balsamifera drought transcriptome. Plant Cell Environ 33:1742–1755. https://doi.org/10.1111/j.1365-3040.2010.02179.x
Hamanishi ET, Barchet GL, Dauwe R et al (2015) Poplar trees reconfigure the transcriptome and metabolome in response to drought in a genotype- and time-of-day-dependent manner. BMC Genom 16:329. https://doi.org/10.1186/s12864-015-1535-z
Harvey HP, Van den Driessche R (1997) Nutrition, xylem cavitation and drought resistance in hybrid poplar. Tree Physiol 17:647–654. https://doi.org/10.1093/treephys/17.10.647
Hogg EHH, Bernier PY (2005) Climate change impacts on drought-prone forests in western Canada. For Chron 81:675–682. https://doi.org/10.5558/tfc81675-5
IPCC (2013) Climate change 2013: the physical science basis. In: Contribution of working group I to the fifth assessment report of the intergovernmental panel on climate change. Cambridge Univ Press, Cambridge, p 1535
Isebrands J, Richardson J (eds) (2014) Poplars and willows: trees for society and the environment. FAO CABI, Rome
Iuchi S, Kobayashi M, Taji T et al (2001) Regulation of drought tolerance by gene manipulation of 9-cis-epoxycarotenoid dioxygenase, a key enzyme in abscisic acid biosynthesis in Arabidopsis. Plant J 27:325–333. https://doi.org/10.1046/j.1365-313X.2001.01096.x
Karp A, Shield I (2008) Bioenergy from plants and the sustainable yield challenge. New Phytol 179:15–32. https://doi.org/10.1111/j.1469-8137.2008.02432.x
Kolosova N, Miller B, Ralph S et al (2004) Isolation of high-quality RNA from gymnosperm and angiosperm trees. Biotechniques 36:821–824
Kreuzwieser J, Hauberg J, Howell KA et al (2009) Differential response of gray poplar leaves and roots underpins stress adaptation during hypoxia. Plant Physiol 149:461–473. https://doi.org/10.1104/pp.108.125989
Kuhn JM, Boisson-Dernier A, Dizon MB, Maktabi MHSJ (2005) The protein phosphatase AtPP2CA negatively regulates abscisic acid signal transduction in arabidopsis, and effects of abh1 on AtPP2CA mRNA. Plant Physiol 140:127–139. https://doi.org/10.1104/pp.105.070318
Larchevêque M, Maurel M, Desrochers A, Larocque GR (2011) How does drought tolerance compare between two improved hybrids of balsam poplar and an unimproved native species? Tree Physiol 31:240–249. https://doi.org/10.1093/treephys/tpr011
Lindquist CH, Cram WH, Howe JAG (1977) Walker poplar. Can J Plant Sci 57:1019
Liu ZJ, Dickmann DI (1992) Abscisic-acid accumulation in leaves of 2 contrasting hybrid poplar clones affected by nitrogen-fertilization plus cyclic flooding and soil drying. Tree Physiol 11:109–122
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2 - ∆∆CT method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262
Ma X, Ma F, Mi Y et al (2008) Morphological and physiological responses of two contrasting Malus species to exogenous abscisic acid application. Plant Growth Regul 56:77–87. https://doi.org/10.1007/s10725-008-9287-2
Marron N, Dreyer E, Boudouresque E et al (2003) Impact of successive drought and re-watering cycles on growth and specific leaf area of two Populus x canadensis (Moench) clones, “Dorskamp” and “Luisa_Avanzo”. Tree Physiol 23:1225–1235. https://doi.org/10.1093/treephys/23.18.1225
Mazzoleni S, Dickmann DI (1988) Differential physiological and morphological responses of two hybrid Populus clones to water stress. Tree Physiol 4:61–70. https://doi.org/10.1093/treephys/4.1.61
McKenney DW, Yemshanov D, Fox G, Ramlal E (2004) Cost estimates for carbon sequestration from fast growing poplar plantations in Canada. For Policy Econ 6:345–358. https://doi.org/10.1016/j.forpol.2004.03.010
Monclus R, Dreyer E, Delmotte FM et al (2005) Productivity, leaf traits and carbon isotope discrimination in 29 Populus deltoides x P. nigra clones. New Phytol 167:53–62. https://doi.org/10.1111/j.1469-8137.2005.01407.x
Monclus R, Dreyer E, Villar M et al (2006) Impact of drought on productivity and water use efficiency in 29 genotypes of Populus deltoides x Populus nigra. New Phytol 169:765–777. https://doi.org/10.1111/j.1469-8137.2005.01630.x
Peng Y, Zhou Z, Tong R et al (2017) Anatomy and ultrastructure adaptations to soil flooding of two full-sib poplar clones differing in flood-tolerance. Flora 233:90–98. https://doi.org/10.1016/J.FLORA.2017.05.014
Plomion C, Lalanne C, Claverol S et al (2006) Mapping the proteome of poplar and application to the discovery of drought-stress responsive proteins. Proteomics 6:6509–6527. https://doi.org/10.1002/pmic.200600362
Regier N, Streb S, Cocozza C et al (2009) Drought tolerance of two black poplar (Populus nigra L.) clones: contribution of carbohydrates and oxidative stress defence. Plant Cell Environ 32:1724–1736. https://doi.org/10.1111/j.1365-3040.2009.02030.x
Robertson GP, Paul EA, Harwood RR (2000) Greenhouse gases in intensive agriculture: contributions of individual gases to the radiative forcing of the atmosphere. Science 289:1922–1952
Rood SB, Patiño S, Coombs K, Tyree MT (2000) Branch sacrifice: cavitation-associated drought adaptation of riparian cottonwoods. Trees Struct Funct 14:248–257. https://doi.org/10.1007/s004680050010
Rood SB, Braatne JH, Hughes FM (2003) Ecophysiology of riparian cottonwoods: stream flow dependency, water relations and restoration. Tree Physiol 23:1113–1124
Rubio S, Rodrigues A, Saez A et al (2009) Triple loss of function of protein phosphatases type 2C leads to partial constitutive response to endogenous abscisic acid. Plant Physiol 150:1345–1355
Saez A, Robert N, Maktabi MH et al (2006) Enhancement of abscisic acid sensitivity and reduction of water consumption in Arabidopsis by combined inactivation of the protein phosphatases Type 2C ABI1 and HAB1. Plant Physiol 141:1389–1399. https://doi.org/10.1104/pp.106.081018
Schindler DW (2009) Lakes as sentinels and integrators for the effects of climate change on watersheds, airsheds, and landscapes. Limnol Oceanogr 54:2349–2358. https://doi.org/10.4319/lo.2009.54.6_part_2.2349
Schindler DW, Donahue WF (2006) An impending water crisis in Canada’s western prairie provinces. Proc Natl Acad Sci 103:7210–7216. https://doi.org/10.1073/pnas.0601568103
Schreiber SG, Hacke UG, Hamann A, Thomas BR (2011) Genetic variation of hydraulic and wood anatomical traits in hybrid poplar and trembling aspen. New Phytol 190:150–160. https://doi.org/10.1111/j.1469-8137.2010.03594.x
Schroeder WR, Lindquist CH (1989) Assiniboine Poplar. Can J Plant Sci 69:351–353. https://doi.org/10.4141/cjps89-046
Secchi F, Zwieniecki MA (2010) Patterns of PIP gene expression in Populus trichocarpa during recovery from xylem embolism suggest a major role for the PIP1 aquaporin subfamily as moderators of refilling process. Plant Cell Environ 33:1285–1297. https://doi.org/10.1111/j.1365-3040.2010.02147.x
Secchi F, Zwieniecki MA (2011) Sensing embolism in xylem vessels: the role of sucrose as a trigger for refilling. Plant Cell Environ 34:514–524. https://doi.org/10.1111/j.1365-3040.2010.02259.x
Secchi F, MacIver B, Zeidel ML, Zwieniecki MA (2009) Functional analysis of putative genes encoding the PIP2 water channel subfamily in Populus trichocarpa. Tree Physiol 29:1467–1477. https://doi.org/10.1093/treephys/tpp060
Secchi F, Pagliarani C, Zwieniecki MA (2017) The functional role of xylem parenchyma cells and aquaporins during recovery from severe water stress. Plant Cell Environ 40:858–871
Seo M, Koshiba T (2002) Complex regulation of ABA biosynthesis in plants. Trends Plant Sci 7:41–48
Silim S, Nash R, Reynard D et al (2009) Leaf gas exchange and water potential responses to drought in nine poplar (Populus spp.) clones with contrasting drought tolerance. Trees Struct Funct 23:959–969. https://doi.org/10.1007/s00468-009-0338-8
Street NR, Skogström O, Sjödin A et al (2006) The genetics and genomics of the drought response in Populus. Plant J 48:321–341. https://doi.org/10.1111/j.1365-313X.2006.02864.x
Talbot P, Thompson SL, Schroeder W, Isabel N (2011) An efficient single nucleotide polymorphism assay to diagnose the genomic identity of poplar species and hybrids on the Canadian prairies. Can J For Res 41:1102–1111. https://doi.org/10.1139/x11-025
Thompson AJ, Jackson AC, Symonds RC et al (2000) Ectopic expression of a tomato 9-cis-epoxycarotenoid dioxygenase gene causes over-production of abscisic acid. Plant J 23:363–374. https://doi.org/10.1046/j.1365-313X.2000.00789.x
Tschaplinski TJ, Tuskan G, Gebre G, Todd D (1998) Drought resistance of two hybrid poplar clones grown in a large scale plantation. Tree Physiol 18:653–658
Viger M, Smith HK, Cohen D et al (2016) Adaptive mechanisms and genomic plasticity for drought tolerance identified in European black poplar (Populus nigra L.). Tree Physiol 36:909–928. https://doi.org/10.1093/treephys/tpw017
Wildhagen H, Paul S, Allwright M et al (2018) Genes and gene clusters related to genotype and drought-induced variation in saccharification potential, lignin content and wood anatomical traits in Populus nigra. Tree Physiol 38:320–339. https://doi.org/10.1093/treephys/tpx054
Wilkins O, Nahal H, Foong J et al (2008) Expansion and diversification of the Populus R2R3-MYB family of transcription factors. Plant Physiol 149:981–993. https://doi.org/10.1104/pp.108.132795
Xiao X, Xu X, Yang F (2008) Adaptive responses to progressive drought stress in two Populus cathayana populations. Silva Fenn 42:705–719
Xiao X, Yang F, Zhang S et al (2009) Physiological and proteomic responses of two contrasting Populus cathayana populations to drought stress. Physiol Plant 136:150–168. https://doi.org/10.1111/j.1399-3054.2009.01222.x
Yuan JS, Tiller KH, Al-Ahmad H et al (2008) Plants to power: bioenergy to fuel the future. Trends Plant Sci 13:421–429. https://doi.org/10.1016/j.tplants.2008.06.001
Acknowledgements
We thank Alberta-Pacific Forest Industries Inc., Alberta, Canada, for providing several hybrid poplar clones and NRC-Plant Biotechnology Institute, Saskatchewan, Canada, for ABA quantifications. Funded by a Natural Sciences and Engineering Research Council of Canada (NSERC; http://www.nserc-crsng.gc.ca/index_eng.asp) Strategic Projects Grant (STPGP 337209-2006) awarded to AP, MC and SDM and by an NSERC discovery grant (RGPIN/05998-2014) to JM. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. We thank the reviewers of this manuscript for their constructive comments.
Author information
Authors and Affiliations
Contributions
AP and JM designed the study, AP, JM and SB supervised and MA and KB carried out the experiments. WRS and BRT provided poplar hybrids. MA and JM analysed the data, JM and MA wrote the manuscript and all authors provided feedback on the manuscript.
Corresponding author
Additional information
Communicated by Rennenberg.
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Arshad, M., Biswas, K., Bisgrove, S. et al. Differences in drought resistance in nine North American hybrid poplars. Trees 33, 1111–1128 (2019). https://doi.org/10.1007/s00468-019-01846-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00468-019-01846-1